He played as a youth for Irish club Manortown United, which was based at Greentrees Park, adjacent to Robert Emmets GAC (it not being unusual in Dublin to play two separate codes of football). After an unsuccessful trial at Fulham he signed professional forms with English club Arsenal in 1983. He was signed as a centre-forward, but also had a brief spell as a centre-half for the Arsenal third team.[11] After scoring 18 goals in 18 reserve matches in the first half of the 1985–86 season, Quinn was included in the first-team squad for a match against Liverpool.[6] Quinn scored in the match as Arsenal recorded a 2–0 win.[12] He made a further 11 league appearances for Arsenal that season, but failed to score as they finished seventh in the league.[13] The end of the season brought Quinn his first call-up to the Republic of Ireland national team.[14]

Quinn found himself playing under a new manager for the following season, as George Graham was appointed in place of Don Howe.[15] Quinn had a regular place in the side that season, appearing in 35 league games and scoring eight goals. He also collected a Football League Cup winner's medal as Arsenal triumphed 2–1 over Liverpool.[16] However, after Arsenal signed another target man, Alan Smith, in the 1987 close season,[17] Quinn struggled to get into the team. Over the next three seasons he managed a total of just 20 league appearances and five goals – his three appearances in 1988–89 not being enough for a title medal. Quinn's lack of opportunities led him to submit a written transfer request at the start of the 1989–90 season.[18] In total he scored 20 goals in 94 appearances for Arsenal, of which 81 were starts.[12]

He managed a total of 193 league appearances in over six years at Maine Road, and scored a total of 64 goals for them.[20]

His most notable game for City was 20 April 1991 when he scored early on and saved a penalty as City beat Derby County 2–1, relegating Derby in the process.[21] City goalkeeper Tony Coton had been sent off before half time for fouling Saunders to concede the penalty. At this time teams rarely named goalkeepers as substitutes, so Quinn replaced Coton in goal. Other notable games included the Manchester derby on 7 November 1993, in which he scored twice in the first half to put City 2–0 up against United by half time, although a remarkable United comeback saw City lose 3–2.[22]

In the 1993 close season, Everton made a bid to sign Quinn and a further bid was made early in the 1993–94 season, but both bids were rejected and Quinn remained at Maine Road for a further three seasons.[23] A cruciate ligament injury sustained in a match against Sheffield Wednesday in November 1993 caused Quinn to miss the majority of the 1993–94 season, and prevented him from playing in the 1994 FIFA World Cup.[7] He returned at the start of the 1994–95 season, but the partnership forged by Uwe Rösler and Paul Walsh in his absence meant he was not always a starter. In attempt to reduce the wage bill, Manchester City tried to sell Quinn in the 1995 close-season, but a proposed move to Lisbon club Sporting fell through after failure to agree contractual terms.[24]

Quinn finished his career with a highly successful spell at Sunderland, joining the north-east club in August 1996 for a club record £1.3 million, although he missed six months of his first season due to a knee injury – similar to the one which ruined his World Cup chances three years earlier. Before his injury, he had got off to a fine start to his Sunderland career, finding the net twice on his debut in a 4–1 win at Nottingham Forest. In his absence from September to March, Sunderland struggled and although he was back in action by the end of the season, they were relegated.[25]

His partnership with striker Kevin Phillips, signed in the 1997 close season, was one of the most prolific in the Football League in the late 1990s and helped the club to promotion to the Premiership. Quinn also has the distinction of being the first player to score at Sunderland's Stadium of Light, against Manchester City in 1997. He became a local legend at Sunderland, winning both the Sunderland and North East Sportswriters' Player of the Year awards in 1999 after scoring 21 goals in Sunderland's record-breaking Division One title-winning season. His final appearance for Sunderland came on 19 October 2002 against West Ham.[26]

Quinn scored the equaliser against the Netherlands in the 1990 World Cup which allowed Ireland to progress to the second round of that tournament. In the qualifiers for the 2002 World Cup he scored against Cyprus on his 35th birthday to break the then national goalscoring record. In the 2002 tournament, his header set up Robbie Keane's late equaliser against Germany, which was the only goal Germany conceded before the final. In the second-round, with Ireland behind 1–0 to Spain, it was a foul on Quinn that led to Ireland's last-minute penalty, converted by Robbie Keane, which tied the game and brought extra-time, but Ireland lost 3–2 in the resulting penalty-shootout.

Quinn had a testimonial match between Sunderland and the Republic of Ireland in 2002. He donated the entire proceeds to charity, an act for which he received a number of awards, including an honorary MBE. Instead of receiving an appearance fee for the game, all the players received a letter from a sick child. Quinn played for both teams during the match, which raised over £1 million. The Republic of Ireland won the match 3 – 0.[27]

Quinn retired in 2003 at the age of 37, taking a brief coaching role at Sunderland. Quinn has also made appearances as a television pundit and commentator for televised matches involving his former teams with Sky Sports.

Heading the Drumaville Consortium of wealthy Irish businessmen, in June 2006 Quinn successfully brokered a deal to buy a controlling stake in Sunderland AFC.[30] In July 2006 Quinn became the chairman and manager of Sunderland.[31] The deal was finalised on 27 July 2006, with sufficient shares being sold to the consortium in order for them to take complete control.

His managerial career did not get off to a good start as the team lost its first four league games in a row. On 22 August Sunderland played Bury away in the League Cup where they lost 2–0.[32] After the match Quinn said that a new manager would be appointed by Sunderland's next game. Contrary to opinion, Niall Quinn didn't sack himself. He was in search of a world class name and stepped to one side (to continue in his role as Sunderland chairman) paving the way for Roy Keane to take charge. This was highly unexpected considering the huge rift between the two arising from Keane's infamous ejection from the 2002 World Cup. Keane was appointed manager of the club on 28 August 2006. The appointment matured into a great success, with Sunderland clinching an immediate Premier League comeback as Football League Championship champions. Quinn has also made substantial amounts of money available for buying new players, as he has a declared ambition to establish Sunderland as a top club.

In October 2011 Ellis Short, the current club owner, replaced Quinn as chairman of Sunderland. Quinn was appointed as Director of International Development on behalf of the club[34] and remained in this role until stepping down in February 2012 and after six years involved with the running of the club saying "Everything is in place for Sunderland to really make a statement, which was always my aim".[35]

Since leaving Sunderland Quinn is now chairman of a satellite broadband company in Ireland called Q Sat.[36]

Quinn has his own song titled "Niall Quinn's Disco Pants". The song was originally created by Manchester City supporters during a night out on a pre-season tour in Penola, Italy. It was 1992. There had been a bust-up with City team-mate Steve McMahon and Quinn had removed his torn and bloodied shirt and was dancing with Rick Holden wearing just a pair of cut-off jeans. He was "hardly aware" that there were a group of hardcore City fans watching and they treated him to "the first performance of the song that will follow me till the end of my career."[10]

Quinn has received praise for his relationship with Sunderland fans. This was highlighted in March 2007 when, during his tenure as chairman, Quinn paid over £8000 to allow around 100 Sunderland fans to travel home by taxi when stranded at Bristol airport after being ejected from their scheduled flight home. The incident happened on Saturday night when Quinn, Sunderland staff and a group of supporters boarded an easyJet flight from Bristol to Newcastle, following Sunderland's 1–0 win at Championship promotion rivals Cardiff. After spotting Quinn, many of the fans broke into song, serenading Quinn with 'Niall Quinn's Disco Pants'. Easyjet staff, angered by the boisterous behaviour, ejected the fans from the plane and Quinn, outraged at the fans' treatment, also left the plane. Quinn, seeing there were no other flights available, decided to commandeer a fleet of taxis and minivans in order to return the fans home.[37]